A multi-trimeric fusion of CD40L and gp100 tumor antigen activates dendritic cells and enhances survival in a B16-F10 melanoma DNA vaccine model

Vaccine

Volumn 33, Issue 38, 2015, Pages 4798-4806

  Gupta, Sachin ^a   Termini, James M ^a   Rivas, Yaelis ^a   Otero, Miguel ^b   Raffa, Francesca N ^a   Bhat, Vikas ^a   Farooq, Amjad ^a   Stone, Geoffrey W ^a  

^a UNIVERSITY OF MIAMI   (United States)

^b UNIVERSITY OF PUERTO RICO   (Puerto Rico)

Author keywords

B16 F10 melanoma; Cancer vaccine; CD40L; Dendritic cell; DNA vaccine; Surfactant protein D

Indexed keywords

CANCER VACCINE; DNA VACCINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR VACCINE; I KAPPA B; INTERLEUKIN 12P70; OLIGOMER; PLASMID DNA; RECOMBINANT GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; RECOMBINANT VACCINE; SURFACTANT PROTEIN D GLYCOPROTEIN GP 100 CD40 LIGAND VACCINE; TUMOR ANTIGEN; UNCLASSIFIED DRUG; CD40 LIGAND; HYBRID PROTEIN; IMMUNOLOGICAL ADJUVANT; MELANOCYTE PROTEIN PMEL 17; SURFACTANT PROTEIN D;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOLOGICAL ACTIVITY; CANCER IMMUNIZATION; CANCER INHIBITION; CANCER MODEL; CANCER SIZE; CANCER SURVIVAL; CELL ACTIVATION; CONTROLLED STUDY; DENDRITIC CELL; DNA IMMUNIZATION; FEMALE; IMMUNE RESPONSE; IN VIVO STUDY; LIGHT SCATTERING; MELANOMA; MOUSE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; DISEASE MODEL; GENETICS; IMMUNOLOGY; METABOLISM; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; CANCER VACCINES; CD40 LIGAND; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FEMALE; GP100 MELANOMA ANTIGEN; MELANOMA; MICE, INBRED C57BL; PULMONARY SURFACTANT-ASSOCIATED PROTEIN D; RECOMBINANT FUSION PROTEINS; SURVIVAL ANALYSIS; TREATMENT OUTCOME; VACCINES, DNA;

EID: 84940718759     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2015.07.081     Document Type: Article

References (47)

1. Begley J., Ribas A. Targeted therapies to improve tumor immunotherapy. Clin Cancer Res 2008, 14(Jul (14)):4385-4391.
2. Jandus C., Speiser D., Romero P. Recent advances and hurdles in melanoma immunotherapy. Pigment Cell Melanoma Res 2009, 22(Dec (6)):711-723.
3. Donnelly J.J., Wahren B., Liu M.A. DNA vaccines: progress and challenges. J Immunol 2005, 175(Jul (2)):633-639.
4. Kutzler M.A., Weiner D.B. DNA vaccines: ready for prime time?. Nat Rev Genet 2008, 9(10):776-788.
5. Melief C.J. Cancer immunotherapy by dendritic cells. Immunity 2008, 29(Sep (3)):372-383.
6. Smith C.A., Farrah T., Goodwin R.G., The T.N.F. receptor superfamily of cellular and viral proteins: activation, costimulation, and death. Cell 1994, 76(Mar (6)):959-962.
7. Abdulhaqq S.A., Weiner D.B. DNA vaccines: developing new strategies to enhance immune responses. Immunol Res 2008, 42(1-3):219-232.
8. Wu L., Kong W.P., Nabel G.J. Enhanced breadth of CD4 T-cell immunity by DNA prime and adenovirus boost immunization to human immunodeficiency virus Env and Gag immunogens. J Virol 2005, 79(Jul (13)):8024-8031.
9. Steinman R.M. Dendritic cells in vivo: a key target for a new vaccine science. Immunity 2008, 29(Sep (3)):319-324.
10. Delamarre L., Holcombe H., Mellman I. Presentation of exogenous antigens on major histocompatibility complex (MHC) class I and MHC class II molecules is differentially regulated during dendritic cell maturation. J Exp Med 2003, 198(Jul (1)):111-122.
11. Chatterjee B., Smed-Sorensen A., Cohn L., Chalouni C., Vandlen R., Lee B.C., et al. Internalization and endosomal degradation of receptor-bound antigens regulate the efficiency of cross presentation by human dendritic cells. Blood 2012, 120(Sep (10)):2011-2020.
12. Cella M., Scheidegger D., Palmer-Lehmann K., Lane P., Lanzavecchia A., Alber G. Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J Exp Med 1996, 184(2):747-752.
13. Schoenberger S.P., Toes R.E., van der Voort E.I., Offringa R., Melief C.J. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 1998, 393(Jun (6684)):480-483.
14. Stone G.W., Barzee S., Snarsky V., Santucci C., Tran B., Langer R., et al. Nanoparticle-delivered multimeric soluble CD40L DNA combined with Toll-Like Receptor agonists as a treatment for melanoma. PLoS ONE 2009, 4(10):e7334.
15. Stone G.W., Barzee S., Snarsky V., Kee K., Spina C.A., Yu X.F., et al. Multimeric soluble CD40 ligand and GITR ligand as adjuvants for human immunodeficiency virus DNA vaccines. J Virol 2006, 80(Feb (4)):1762-1772.
16. Crouch E., Persson A., Chang D., Heuser J. Molecular structure of pulmonary surfactant protein D (SP-D). J Biol Chem 1994, 269(25):17311-17319.
17. Rakhmilevich A.L., Turner J., Ford M.J., McCabe D., Sun W.H., Sondel P.M., et al. Gene gun-mediated skin transfection with interleukin 12 gene results in regression of established primary and metastatic murine tumors. Proc Natl Acad Sci USA 1996, 93(Jun (13)):6291-6296.
18. Jager E., Ringhoffer M., Dienes H.P., Arand M., Karbach J., Jager D., et al. Granulocyte-macrophage-colony-stimulating factor enhances immune responses to melanoma-associated peptides in vivo. Int J Cancer 1996, 67(Jul (1)):54-62.
19. Chattergoon M.A., Saulino V., Shames J.P., Stein J., Montaner L.J., Weiner D.B. Co-immunization with plasmid IL-12 generates a strong T-cell memory response in mice. Vaccine 2004, 22(Apr (13-14)):1744-1750.
20. Xu R., Megati S., Roopchand V., Luckay A., Masood A., Garcia-Hand D., et al. Comparative ability of various plasmid-based cytokines and chemokines to adjuvant the activity of HIV plasmid DNA vaccines. Vaccine 2008, 26(Sep (37)):4819-4829.
21. Lou Y., Wang G., Lizee G., Kim G.J., Finkelstein S.E., Feng C., et al. Dendritic cells strongly boost the antitumor activity of adoptively transferred T cells in vivo. Cancer Res 2004, 64(Sep (18)):6783-6790.
22. Bhat V., Olenick M.B., Schuchardt B.J., Mikles D.C., Deegan B.J., McDonald C.B., et al. Heat-induced fibrillation of BclXL apoptotic repressor. Biophys Chem 2013, 179(Sep):12-25.
23. Wyatt P.J. Light scattering and the absolute characterization of macromolecules. Anal Chim Acta 1993, 272:1-40.
24. Chu B. Laser light scattering: basic principles and practice 1991, Academic, Boston, MA.
25. Maurais E., Cantin R., Tremblay M.J. Human immunodeficiency virus type 1-anchored CD40 ligand induces secretion of the chemokine interleukin-8 by human primary macrophages. Virology 2009, 385(Mar (1)):227-232.
26. Inaba K., Inaba M., Romani N., Aya H., Deguchi M., Ikehara S., et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med 1992, 176(6):1693-1702.
27. Quezada S.A., Peggs K.S., Curran M.A., Allison J.P. CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells. J Clin Invest 2006, 116(7):1935-1945.
28. van Mierlo G.J., den Boer A.T., Medema J.P., van der Voort E.I., Fransen M.F., Offringa R., et al. CD40 stimulation leads to effective therapy of CD40(-) tumors through induction of strong systemic cytotoxic T lymphocyte immunity. Proc Natl Acad Sci USA 2002, 99(Apr (8)):5561-5566.
29. French R.R., Chan H.T., Tutt A.L., Glennie M.J. CD40 antibody evokes a cytotoxic T-cell response that eradicates lymphoma and bypasses T-cell help. Nat Med 1999, 5(5):548-553.
30. Sotomayor E.M., Borrello I., Tubb E., Rattis F.M., Bien H., Lu Z., et al. Conversion of tumor-specific CD4+ T-cell tolerance to T-cell priming through in vivo ligation of CD40. Nat Med 1999, 5(7):780-787.
31. Bachmann M.F., Schwarz K., Wolint P., Meijerink E., Martin S., Manolova V., et al. Cutting edge: distinct roles for T help and CD40/CD40 ligand in regulating differentiation of proliferation-competent memory CD8+ T cells. J Immunol 2004, 173(Aug (4)):2217-2221.
32. Fujii S., Liu K., Smith C., Bonito A.J., Steinman R.M. The linkage of innate to adaptive immunity via maturing dendritic cells in vivo requires CD40 ligation in addition to antigen presentation and CD80/86 costimulation. J Exp Med 2004, 199(Jun (12)):1607-1618.
33. Bonifaz L.C., Bonnyay D.P., Charalambous A., Darguste D.I., Fujii S., Soares H., et al. In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination. J Exp Med 2004, 199(Mar (6)):815-824.
34. Kanagavelu S.K., Snarsky V., Termini J.M., Gupta S., Barzee S., Wright J.A., et al. Soluble multi-trimeric TNF superfamily ligand adjuvants enhance immune responses to a HIV-1 Gag DNA vaccine. Vaccine 2012, 30(Jan (4)):691-702.
35. Haswell L.E., Glennie M.J., Al-Shamkhani A. Analysis of the oligomeric requirement for signaling by CD40 using soluble multimeric forms of its ligand CD154. Eur J Immunol 2001, 31(10):3094-3100.
36. Grosso J.F., Jure-Kunkel M.N. CTLA-4 blockade in tumor models: an overview of preclinical and translational research. Cancer Immunol 2013, 13:5.
37. Sheikh N.A., Petrylak D., Kantoff P.W., Dela Rosa C., Stewart F.P., Kuan L.Y., et al. Sipuleucel-T immune parameters correlate with survival: an analysis of the randomized phase 3 clinical trials in men with castration-resistant prostate cancer. Cancer Immunol Immunother 2013, 62(1):137-147.
38. Terando A.M., Faries M.B., Morton D.L. Vaccine therapy for melanoma: current status and future directions. Vaccine 2007, 25(Sep (Suppl. 2)):B4-B16.
39. Bloom M.B., Perry-Lalley D., Robbins P.F., Li Y., el-Gamil M., Rosenberg S.A., et al. Identification of tyrosinase-related protein 2 as a tumor rejection antigen for the B16 melanoma. J Exp Med 1997, 185(Feb (3)):453-459.
40. de Vries T.J., Fourkour A., Wobbes T., Verkroost G., Ruiter D.J., van Muijen G.N. Heterogeneous expression of immunotherapy candidate proteins gp100 MART-1, and tyrosinase in human melanoma cell lines and in human melanocytic lesions. Cancer Res 1997, 57(Aug (15)):3223-3229.
41. Rice J., Ottensmeier C.H., Stevenson F.K. DNA vaccines: precision tools for activating effective immunity against cancer. Nat Rev Cancer 2008, 8(2):108-120.
42. Chattergoon M.A., Robinson T.M., Boyer J.D., Weiner D.B. Specific immune induction following DNA-based immunization through in vivo transfection and activation of macrophages/antigen-presenting cells. J Immunol 1998, 160(Jun (12)):5707-5718.
43. Stone G.W., Barzee S., Snarsky V., Spina C.A., Lifson J.D., Pillai V.K., et al. Macaque multimeric soluble CD40 ligand and GITR ligand constructs are immunostimulatory molecules in vitro. Clin Vaccine Immunol 2006, 13(11):1223-1230.
44. Fidler I.J. Biological behavior of malignant melanoma cells correlated to their survival in vivo. Cancer Res 1975, 35(1):218-224.
45. Frumento G., Piazza T., Di Carlo E., Ferrini S. Targeting tumor-related immunosuppression for cancer immunotherapy. Endocr Metab Immune Disord Drug Targets 2006, 6(Sep (3)):233-237.
46. Kim R., Emi M., Tanabe K. Functional roles of immature dendritic cells in impaired immunity of solid tumour and their targeted strategies for provoking tumour immunity. Clin Exp Immunol 2006, 146(Nov (2)):189-196.
47. Gupta S., Termini J.M., Raffa F.N., Williams C.A., Kornbluth R.S., Stone G.W. Vaccination with a fusion protein that introduces HIV-1 gag antigen into a multitrimer CD40L construct results in enhanced CD8+ T cell responses and protection from viral challenge by vaccinia-gag. J Virol 2014, 88(Feb (3)):1492-1501.